The Succession star, who won the award for Best Actor in a Drama Series for his performance as the mischievous, foul-mouthed Roman Roy, used his speech to tell Charton: “Thank you for sharing your life with me and giving me two amazing kids… I want more. You said ‘maybe’, if I win! I love you so much.”
In response, Charton could be seen covering her face with her hands in a mixture of joy and shock.
Culkin, 41, and Charton, 35, share two children together: Kinsey Sioux and Wilder Wolf.
The actor also thanked his agent in his emotional speech, saying: “I have to thank my manager, Emily Gerson Saines, who I’ve been with about 29 years. Sorry Emily, you probably didn’t want me to say the number but I did. I just have to thank you for keeping my name in the conversation when nobody else was talking about me, so as far as I’m concerned, this is yours.”
Earlier in the evening, Pedro Pascal issued a cheeky retort to Culkin while presenting the award for Best Supporting Actor in a Drama Series.
Culkin had previously told the Last of Us actor to “suck it” while accepting the Golden Globe for Best Actor in a Drama earlier this month.
At the Emmys, Pascal, 48, was seen wearing a sling around his arm, having sustained an injury to his shoulder.
He told the crowd: “A lot of people have been asking about my arm, it’s actually my shoulder… Kieran Culkin beat the s*** out of me.”
The Emmys, held at the Peacock Theater in Los Angeles, was delayed by four months due to the writers’ and actors’ strikes last year.
Succession went into the night as the favourite throughout most of the drama categories, and ended the evening with six wins.
The series, which concluded its fourth and final season last May, focused on the power struggles within a family of media moguls.
You can find a list of all the night’s winners here.